MeCP2 links heterochromatin condensates and neurodevelopmental disease.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
10 2020
Historique:
received: 31 07 2019
accepted: 15 07 2020
pubmed: 23 7 2020
medline: 15 12 2020
entrez: 23 7 2020
Statut: ppublish

Résumé

Methyl CpG binding protein 2 (MeCP2) is a key component of constitutive heterochromatin, which is crucial for chromosome maintenance and transcriptional silencing

Identifiants

pubmed: 32698189
doi: 10.1038/s41586-020-2574-4
pii: 10.1038/s41586-020-2574-4
pmc: PMC7735819
mid: NIHMS1646018
doi:

Substances chimiques

Heterochromatin 0
MECP2 protein, human 0
Methyl-CpG-Binding Protein 2 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

440-444

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM123511
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007287
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH104610
Pays : United States
Organisme : NIH HHS
ID : 2 R01 MH104610-20
Pays : United States
Organisme : NIMH NIH HHS
ID : K99 MH113813
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM087237
Pays : United States
Organisme : NIMH NIH HHS
ID : R00 MH113813
Pays : United States
Organisme : NCI NIH HHS
ID : R37 CA084198
Pays : United States
Organisme : NIH HHS
ID : T32 5T3DK007191-45
Pays : United States
Organisme : NIDDK NIH HHS
ID : T32 DK007191
Pays : United States

Références

Janssen, A., Colmenares, S. U. & Karpen, G. H. Heterochromatin: guardian of the genome. Annu. Rev. Cell Dev. Biol. 34, 265–288 (2018).
pubmed: 30044650
Allshire, R. C. & Madhani, H. D. Ten principles of heterochromatin formation and function. Nat. Rev. Mol. Cell Biol. 19, 229–244 (2018).
pubmed: 29235574
Lyst, M. J. & Bird, A. Rett syndrome: a complex disorder with simple roots. Nat. Rev. Genet. 16, 261–275 (2015).
pubmed: 25732612
Ip, J. P. K., Mellios, N. & Sur, M. Rett syndrome: insights into genetic, molecular and circuit mechanisms. Nat. Rev. Neurosci. 19, 368–382 (2018).
pubmed: 29740174 pmcid: 6402579
Amir, R. E. et al. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 23, 185–188 (1999).
pubmed: 10508514
Larson, A. G. et al. Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin. Nature 547, 236–240 (2017).
pubmed: 28636604 pmcid: 5606208
Strom, A. R. et al. Phase separation drives heterochromatin domain formation. Nature 547, 241–245 (2017).
pubmed: 28636597 pmcid: 6022742
Skene, P. J. et al. Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol. Cell 37, 457–468 (2010).
pubmed: 20188665 pmcid: 4338610
Shrinivas, K. et al. Enhancer features that drive formation of transcriptional condensates. Mol. Cell 75, 549–561.e7 (2019).
pubmed: 31398323 pmcid: 6690378
Shin, Y. & Brangwynne, C. P. Liquid phase condensation in cell physiology and disease. Science 357, eaaf4382 (2017).
pubmed: 28935776
Kumar, A. et al. Analysis of protein domains and Rett syndrome mutations indicate that multiple regions influence chromatin-binding dynamics of the chromatin-associated protein MECP2 in vivo. J. Cell Sci. 121, 1128–1137 (2008).
pubmed: 18334558
Georgel, P. T. et al. Chromatin compaction by human MeCP2. Assembly of novel secondary chromatin structures in the absence of DNA methylation. J. Biol. Chem. 278, 32181–32188 (2003).
pubmed: 12788925
Lyst, M. J. et al. Rett syndrome mutations abolish the interaction of MeCP2 with the NCoR/SMRT co-repressor. Nat. Neurosci. 16, 898–902 (2013).
pubmed: 23770565
Nan, X., Campoy, F. J. & Bird, A. MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88, 471–481 (1997).
pubmed: 9038338
Baker, S. A. et al. An AT-hook domain in MeCP2 determines the clinical course of Rett syndrome and related disorders. Cell 152, 984–996 (2013).
pubmed: 23452848 pmcid: 3641682
Sabari, B. R. et al. Coactivator condensation at super-enhancers links phase separation and gene control. Science 361, eaar3958 (2018).
pubmed: 29930091 pmcid: 6092193
Boija, A. et al. Transcription factors activate genes through the phase-separation capacity of their activation domains. Cell 175, 1842–1855.e16 (2018).
pubmed: 30449618
van Steensel, B. & Belmont, A. S. Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression. Cell 169, 780–791 (2017).
pubmed: 28525751 pmcid: 5532494
Gibson, B. A. et al. Organization of chromatin by intrinsic and regulated phase separation. Cell 179, 470–484.e21 (2019).
pubmed: 31543265 pmcid: 6778041
Chahrour, M. et al. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320, 1224–1229 (2008).
pubmed: 18511691 pmcid: 2443785
Kruusvee, V. et al. Structure of the MeCP2-TBLR1 complex reveals a molecular basis for Rett syndrome and related disorders. Proc. Natl Acad. Sci. USA 114, E3243–E3250 (2017).
pubmed: 28348241 pmcid: 5402415
Tillotson, R. et al. Radically truncated MeCP2 rescues Rett syndrome-like neurological defects. Nature 550, 398–401 (2017).
pubmed: 29019980 pmcid: 5884422
Linhoff, M. W., Garg, S. K. & Mandel, G. A high-resolution imaging approach to investigate chromatin architecture in complex tissues. Cell 163, 246–255 (2015).
pubmed: 26406379 pmcid: 4583660
Li, Y. et al. Global transcriptional and translational repression in human-embryonic-stem-cell-derived Rett syndrome neurons. Cell Stem Cell 13, 446–458 (2013).
pubmed: 24094325 pmcid: 4053296
Wang, L. et al. Rett syndrome-causing mutations compromise MeCP2-mediated liquid-liquid phase separation of chromatin. Cell Res. 30, 393–407 (2020).
pubmed: 32111972 pmcid: 7196128
Brown, K. et al. The molecular basis of variable phenotypic severity among common missense mutations causing Rett syndrome. Hum. Mol. Genet. 25, 558–570 (2016).
pubmed: 26647311
Guy, J., Gan, J., Selfridge, J., Cobb, S. & Bird, A. Reversal of neurological defects in a mouse model of Rett syndrome. Science 315, 1143–1147 (2007).
pubmed: 17289941 pmcid: 7610836
Giacometti, E., Luikenhuis, S., Beard, C. & Jaenisch, R. Partial rescue of MeCP2 deficiency by postnatal activation of MeCP2. Proc. Natl Acad. Sci. USA 104, 1931–1936 (2007).
pubmed: 17267601 pmcid: 1794312
Wheeler, R. J. et al. Small molecules for modulating protein driven liquid-liquid phase separation in treating neurodegenerative disease. Preprint at  https://www.biorxiv.org/content/10.1101/721001v2  (2019).
Klein, I. A. et al. Partitioning of cancer therapeutics in nuclear condensates. Science 368, 1386–1392 (2020).
pubmed: 32554597 pmcid: 7735713
Thoma, E. C. et al. Ectopic expression of neurogenin 2 alone is sufficient to induce differentiation of embryonic stem cells into mature neurons. PLoS ONE 7, e38651 (2012).
pubmed: 22719915 pmcid: 3374837
Zhang, Y. et al. Rapid single-step induction of functional neurons from human pluripotent stem cells. Neuron 78, 785–798 (2013).
pubmed: 23764284 pmcid: 3751803
Alberti, S., Gladfelter, A. & Mittag, T. Considerations and challenges in studying liquid-liquid phase separation and biomolecular condensates. Cell 176, 419–434 (2019).
pubmed: 30682370 pmcid: 6445271
Jang, S. et al. Long-term culture of organotypic hippocampal slice from old 3xTg-AD mouse: an ex vivo model of Alzheimer’s disease. Psychiatry Investig. 15, 205–213 (2018).
pubmed: 29475217
Alberti, S. et al. A user’s guide for phase separation assays with purified proteins. J. Mol. Biol. 430, 4806–4820 (2018).
pubmed: 29944854 pmcid: 6215329
Wang, J. et al. A molecular grammar governing the driving forces for phase separation of prion-like RNA binding proteins. Cell 174, 688–699.e16 (2018).
pubmed: 29961577 pmcid: 6063760
Loyola, A., Bonaldi, T., Roche, D., Imhof, A. & Almouzni, G. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol. Cell 24, 309–316 (2006).
pubmed: 17052464
Li, P. et al. Phase transitions in the assembly of multivalent signalling proteins. Nature 483, 336–340 (2012).
pubmed: 22398450 pmcid: 3343696
Martin, E. W. et al. Valence and patterning of aromatic residues determine the phase behavior of prion-like domains. Science 367, 694–699 (2020).
pubmed: 32029630 pmcid: 7297187
Lu, H. et al. Phase-separation mechanism for C-terminal hyperphosphorylation of RNA polymerase II. Nature 558, 318–323 (2018).
pubmed: 29849146 pmcid: 6475116
Zamudio, A. V. et al. Mediator condensates localize signaling factors to key cell kdentity genes. Mol. Cell 76, 753–766.e6 (2019).
pubmed: 31563432 pmcid: 6898777
Pak, C. W. et al. Sequence determinants of intracellular phase separation by complex coacervation of a disordered protein. Mol. Cell 63, 72–85 (2016).
pubmed: 27392146 pmcid: 4973464
Dao, T. P. et al. ALS-linked mutations affect UBQLN2 oligomerization and phase separation in a position- and amino acid-dependent manner. Structure 27, 937–951.e5 (2019).
pubmed: 30982635 pmcid: 6551275
Holehouse, A. S., Das, R. K., Ahad, J. N., Richardson, M. O. G. & Pappu, R. V. CIDER: resources to analyze sequence-ensemble relationships of intrinsically disordered proteins. Biophys. J. 112, 16–21 (2017).
pubmed: 28076807 pmcid: 5232785
Lovén, J. et al. Revisiting global gene expression analysis. Cell 151, 476–482 (2012).
pubmed: 23101621 pmcid: 3505597
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886
Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323 (2011).
pubmed: 21816040 pmcid: 3163565
Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
pubmed: 20979621 pmcid: 3218662
Christodoulou, J., Grimm, A., Maher, T. & Bennetts, B. RettBASE: The IRSA MECP2 variation database-a new mutation database in evolution. Hum. Mutat. 21, 466–472 (2003).
pubmed: 12673788
Capra, J. A. & Singh, M. Predicting functionally important residues from sequence conservation. Bioinformatics 23, 1875–1882 (2007).
pubmed: 17519246

Auteurs

Charles H Li (CH)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.
Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.

Eliot L Coffey (EL)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.
Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.

Alessandra Dall'Agnese (A)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.

Nancy M Hannett (NM)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.

Xin Tang (X)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.

Jonathan E Henninger (JE)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.

Jesse M Platt (JM)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.
Division of Gastroenterology, Department of Medicine, Massachusetts General Hospital, Boston, MA, USA.

Ozgur Oksuz (O)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.

Alicia V Zamudio (AV)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.
Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.

Lena K Afeyan (LK)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.
Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.

Jurian Schuijers (J)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.
Center for Molecular Medicine, University Medical Center Utrecht, Utrecht, The Netherlands.

X Shawn Liu (XS)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.
Department of Physiology and Cellular Biophysics, Columbia University Medical Center, New York, NY, USA.

Styliani Markoulaki (S)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.

Tenzin Lungjangwa (T)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.

Gary LeRoy (G)

Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY, USA.

Devon S Svoboda (DS)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.

Emile Wogram (E)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.

Tong Ihn Lee (TI)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.

Rudolf Jaenisch (R)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA. jaenisch@wi.mit.edu.
Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA. jaenisch@wi.mit.edu.

Richard A Young (RA)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA. young@wi.mit.edu.
Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA. young@wi.mit.edu.

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